Direct evidence for activity-dependent glucose phosphorylation in neurons with implications for the astrocyte-to-neuron lactate shuttle
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Previous (13)C magnetic resonance spectroscopy experiments have shown that over a wide range of neuronal activity, approximately one molecule of glucose is oxidized for every molecule of glutamate released by neurons and recycled through astrocytic glutamine. The measured kinetics were shown to agree with the stoichiometry of a hypothetical astrocyte-to-neuron lactate shuttle model, which predicted negligible functional neuronal uptake of glucose. To test this model, we measured the uptake and phosphorylation of glucose in nerve terminals isolated from rats infused with the glucose analog, 2-fluoro-2-deoxy-D-glucose (FDG) in vivo. The concentrations of phosphorylated FDG (FDG6P), normalized with respect to known neuronal metabolites, were compared in nerve terminals, homogenate, and cortex of anesthetized rats with and without bicuculline-induced seizures. The increase in FDG6P in nerve terminals agreed well with the increase in cortical neuronal glucose oxidation measured previously under the same conditions in vivo, indicating that direct uptake and oxidation of glucose in nerve terminals is substantial under resting and activated conditions. These results suggest that neuronal glucose-derived pyruvate is the major oxidative fuel for activated neurons, not lactate-derived from astrocytes, contradicting predictions of the original astrocyte-to-neuron lactate shuttle model under the range of study conditions.
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In vivo uptake of 2-fluoro-2-DG into presynaptic terminals of rat brain indicated substantial direct metabolism of glucose.
“In vivo uptake of 2-fluoro–2-DG into presynaptic terminals of rat brain assessed by postmortem isolation of synaptosomes (Patel et al., 2014) indicated substantial direct metabolism of glucose”
From Fueling thought: Management of glycolysis and oxidative phosphorylation in neuronal metabolism (2018) · cites this paper as Patel et al., 2014
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- Authors
- Patel, A. B., Lai, J. C. K., Chowdhury, G. M. I., Hyder, F., Rothman, D. L., Shulman, R. G., & Behar, K. L.
- Affiliations
- Centre for Cellular and Molecular Biology (IN)
- Idaho State University (US)
- Magnetic Resonance Research Center and
- Yale University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-03-26
- Volume
- 111
- Issue
- 14
- Pages
- 5385-5390
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3986127
- OpenAlex
- W2111261869
- Cited by
- 186
- References
- 61
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 10 · 2023: 18 · 2022: 13 · 2021: 12 · 2020: 7 · 2019: 17 · 2018: 16 · 2017: 25 · 2016: 21 · 2015: 25 · 2014: 8
- FWCI
- 12.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (R01-DK27121, R01-DK27121-28S, R01DK027121)
- National Institute of Neurological Disorders and Stroke (P30NS052519)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Keywords
- neuronal glucose uptake, glucose phosphorylation, presynaptic terminals, 2-fluoro-2-deoxy-D-glucose, bicuculline-induced seizures, pyruvate, glutamate release, astrocytes, brain energy metabolism
- MeSH terms
- Animals, Astrocytes, Glucose, Neurons, Phosphorylation, Lactic Acid, Rats
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